Characterization of protamine uptake by opossum kidney epithelial cells

Biological and Pharmaceutical Bulletin

Volumn 36, Issue 12, 2013, Pages 1942-1949

  Nagai, Junya ^a   Komeda, Takuji ^a   Katagiri, Yuki ^a   Yumoto, Ryoko ^a   Takano, Mikihisa ^a  

^a HIROSHIMA UNIVERSITY   (Japan)

Author keywords

Endocytosis; Opossum kidney cell; Polycationic drug; Protamine; Renal proximal tubular cell

Indexed keywords

ARGININE; CAVEOLIN; CLATHRIN; FLUORESCEIN ISOTHIOCYANATE; GENTAMICIN; HEPARIN LYASE; HEPARINASE III; POLYMYXIN B; PROTAMINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CELL TRANSPORT; CELLULAR DISTRIBUTION; CONCENTRATION RESPONSE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; ENDOCYTOSIS; ENERGY METABOLISM; FLOW CYTOMETRY; FLUORESCENCE ANALYSIS; IN VITRO STUDY; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE CELL; NONHUMAN; OPOSSUM; PROTEIN TRANSPORT; SALMON; TEMPERATURE SENSITIVITY;

ANIMALS; CELLS, CULTURED; ENDOCYTOSIS; EPITHELIAL CELLS; FLUORESCEIN-5-ISOTHIOCYANATE; FLUORESCENT DYES; HEPARIN ANTAGONISTS; KIDNEY; MALE; MICROVILLI; OPOSSUMS; PROTAMINES; RATS; RATS, WISTAR;

EID: 84892602289     PISSN: 09186158     EISSN: 13475215     Source Type: Journal    
DOI: 10.1248/bpb.b13-00553     Document Type: Article

References (35)

1. Jaques LB. Protamine-antagonist to heparin. Can. Med. Assoc. J., 108, 1291-1297 (1973).
2. Owens DR. Insulin preparations with prolonged effect. Diabetes Technol. Ther., 13 (Suppl. , S5-S14 (2011).
3. Sorgi FL, Bhattacharya S, Huang L. Protamine sulfate enhances lipid-mediated gene transfer. Gene Ther., 4, 961-968 (1997).
4. Junghans M, Kreuter J, Zimmer A. Antisense delivery using protamine-oligonucleotide particles. Nucleic Acids Res., 28, E45 (2000).
5. Reynolds F, Weissleder R, Josephson L. Protamine as an efficient membrane-translocating peptide. Bioconjug. Chem., 16, 1240-1245 (2005).
6. DeLucia A 3rd, Wakefield TW, Kadell AM, Wrobleski SK, VanDort M, Stanley JC. Tissue distribution, circulating half-life, and excretion of intravenously administered protamine sulfate. ASAIO J., 39, M715-M718 (1993).
7. Butterworth J, Lin YA, Prielipp R, Bennett J, James R. The pharmacokinetics and cardiovascular effects of a single intravenous dose of protamine in normal volunteers. Anesth. Analg., 94, 514-522 (2002).
8. Butterworth J, Lin YA, Prielipp RC, Bennett J, Hammon JW, James RL. Rapid disappearance of protamine in adults undergoing cardiac operation with cardiopulmonary bypass. Ann. Thorac. Surg., 74, 1589-1595 (2002).
9. Nagai J, Komeda T, Yumoto R, Takano M. Effect of protamine on the accumulation of gentamicin in opossum kidney epithelial cells. J. Pharm. Pharmacol., 65, 441-446 (2013).
10. Zhai XY, Nielsen R, Birn H, Drumm K, Mildenberger S, Freudinger R, Moestrup SK, Verroust PJ, Christensen EI, Gekle M. Cubilin-and megalin-mediated uptake of albumin in cultured proximal tubule cells of opossum kidney. Kidney Int., 58, 1523-1533 (2000).
11. Christensen EI, Birn H. Megalin and cubilin: multifunctional endocytic receptors. Nat. Rev. Mol. Cell Biol., 3, 256-266 (2002).
12. Christensen EI, Verroust PJ, Nielsen R. Receptor-mediated endocytosis in renal proximal tubule. Pflugers Arch., 458, 1039-1048 (2009).
13. Park YJ, Liang JF, Ko KS, Kim SW, Yang VC. Low molecular weight protamine as an efficient and nontoxic gene carrier: in vitro study. J. Gene Med., 5, 700-711 (2003).
14. Lee TY, Park YS, Garcia GA, Sunahara RK, Woods JH, Yang VC. Cell permeable cocaine esterases constructed by chemical conjugation and genetic recombination. Mol. Pharm., 9, 1361-1373 (2012).
15. Handler JS. Studies of kidney cells in culture. Kidney Int., 30, 208-215 (1986).
16. Takano M, Hirozane K, Okamura M, Takayama A, Nagai J, Hori R. p-Aminohippurate transport in apical and basolateral membranes of the OK kidney epithelial cells. J. Pharmacol. Exp. Ther., 269, 970-975 (1994).
17. Schwegler JS, Heppelmann B, Mildenberger S, Silbernagl S. Receptor-mediated endocytosis of albumin in cultured opossum kidney cells: a model for proximal tubular protein reabsorption. Pflugers Arch., 418, 383-392 (1991).
18. Nagai J, Saito M, Adachi Y, Yumoto R, Takano M. Inhibition of gentamicin binding to rat renal brush-border membrane by megalin ligands and basic peptides. J. Control. Release, 112, 43-50 (2006).
19. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72, 248-254 (1976).
20. Nagai J, Sato K, Yumoto R, Takano M. Megalin/cubilin-mediated uptake of FITC-labeled IgG by OK kidney epithelial cells. Drug Metab. Pharmacokinet., 26, 474-485 (2011).
21. Richard JP, Melikov K, Vives E, Ramos C, Verbeure B, Gait MJ, Chernomordik LV, Lebleu B. Cell-penetrating peptides. A reevaluation of the mechanism of cellular uptake. J. Biol. Chem., 278, 585-590 (2003).
22. Green I, Christison R, Voyce CJ, Bundell KR, Lindsay MA. Protein transduction domains: are they delivering? Trends Pharmacol. Sci., 24, 213-215 (2003).
23. Fretz M, Jin J, Conibere R, Penning NA, Al-Taei S, Storm G, Futaki S, Takeuchi T, Nakase I, Jones AT. Effects of Na+/H+ exchanger inhibitors on subcellular localisation of endocytic organelles and intracellular dynamics of protein transduction domains HIV-TAT peptide and octaarginine. J. Control. Release, 116, 247-254 (2006).
24. Moestrup SK, Cui S, Vorum H, Bregengård C, Bjørn SE, Norris K, Gliemann J, Christensen EI. Evidence that epithelial glycoprotein 330/megalin mediates uptake of polybasic drugs. J. Clin. Invest., 96, 1404-1413 (1995).
25. Vaara M, Fox J, Loidl G, Siikanen O, Apajalahti J, Hansen F, Frimodt-Møller N, Nagai J, Takano M, Vaara T. Novel polymyxin derivatives carrying only three positive charges are effective antibacterial agents. Antimicrob. Agents Chemother., 52, 3229-3236 (2008).
26. Tyagi M, Rusnati M, Presta M, Giacca M. Internalization of HIV-1 tat requires cell surface heparan sulfate proteoglycans. J. Biol. Chem., 276, 3254-3261 (2001).
27. Duchardt F, Fotin-Mleczek M, Schwarz H, Fischer R, Brock R. A comprehensive model for the cellular uptake of cationic cell-penetrating peptides. Traffic, 8, 848-866 (2007).
28. Jones SW, Christison R, Bundell K, Voyce CJ, Brockbank SM, Newham P, Lindsay MA. Characterisation of cell-penetrating peptide-mediated peptide delivery. Br. J. Pharmacol., 145, 1093-1102 (2005).
29. Yanai S, Sugiyama Y, Iga T, Fuwa T, Hanano M. Kinetic analysis of the downregulation of epidermal growth factor receptors in rats in vivo. Am. J. Physiol., 258, C593-C598 (1990).
30. Liu KX, Kato Y, Kino I, Nakamura T, Sugiyama Y. Ligand-induced downregulation of receptor-mediated clearance of hepatocyte growth factor in rats. Am. J. Physiol., 275, E835-E842 (1998).
31. Mayor S, Pagano RE. Pathways of clathrin-independent endocytosis. Nat. Rev. Mol. Cell Biol., 8, 603-612 (2007).
32. Ivanov AI, Nusrat A, Parkos CA. Endocytosis of epithelial apical junctional proteins by a clathrin-mediated pathway into a unique storage compartment. Mol. Biol. Cell, 15, 176-188 (2004).
33. Ivanov AI. Pharmacological inhibition of endocytic pathways: is it specific enough to be useful? Methods Mol. Biol., 440, 15-33 (2008).
34. Richard JP, Melikov K, Brooks H, Prevot P, Lebleu B, Chernomordik LV. Cellular uptake of unconjugated TAT peptide involves clathrin-dependent endocytosis and heparan sulfate receptors. J. Biol. Chem., 280, 15300-15306 (2005).
35. Tauris J, Christensen EI, Nykjaer A, Jacobsen C, Petersen CM, Ovesen T. Cubilin and megalin co-localize in the neonatal inner ear. Audiol. Neurootol., 14, 267-278 (2009).